Effect of breathing conditions on relationships between impairment, breathing laterality and coordination symmetry in elite para swimmers

The aim was to investigate the effect of breathing conditions and swimming pace on the relationships between the impairment, the breathing laterality and motor coordination symmetry in elite front crawl Para swimmers. Fifteen elite Para swimmers with unilateral physical impairment or with visual impairment and unilateral breathing preference performed eight 25 m using four breathing conditions (every three strokes, every two strokes on preferred and non-preferred breathing side and apnea) at slow and fast paces in a randomized order. Multicamera video system and five sensors have been used to assess arm and leg stroke phases and to compute symmetry of arm coordination (SIIdC) and of leg kick rate (SIKR). Our findings emphasized motor coordination asymmetry whatever the breathing conditions and swimming paces, highlighting the influence of impairment. Multinomial logistic regression exhibited a high probability for motor coordination asymmetry (SIIdC and SIKR) to be present in categories of Para swimmers with impairment and breathing laterality on the same side, suggesting the joined effect of unilateral impairment and unilateral breathing. Moreover, unilateral physical impairment and breathing laterality could also occur on different sides and generate motor coordination asymmetry on different sides and different levels (arms vs. legs). Finally, visual impairment seems amplify the effect of unilateral breathing on motor coordination asymmetry.


Effect of breathing conditions and swimming paces on stroking parameters and motor coordination
The two-way repeated measures ANOVA did not show any significant differences of the breathing conditions nor any significant interaction between the breathing conditions and the swimming paces on the stroking parameters and motor coordination (Table 1).On the average of the four breathing conditions, the two-way repeated measures ANOVA showed significant higher speeds (1.48 ± 0.17 m s −1 ) at fast pace than at slow pace (1.16 ± 0.13 m s −1 ) (F 1,13 = 38.11,p < 0.001, η P 2 = 0.746), which correspond to an increase of 78% between the slow and fast pace (knowing that a minimum of 40% was expected).The two-way repeated measures ANOVA also showed significant higher stroke rate (F 1,13 = 93.39,p < 0.001, η P 2 = 0.878), higher stroke length (F 1,13 = 37.05, p < 0.001, η P 2 = 0.74), higher index of coordination (IdC) (F 1,13 = 11.63,p = 0.005, η P 2 = 0.472) and higher leg kicking rate (KR) (F 1,13 = 11.14, p = 0.007, η P 2 = 0.503) at fast pace than at slow pace, but no significant effect of swimming paces on SI IDC and SI KR .Taken together, the results of SI IDC and SI KR exhibited asymmetric arm coordination and asymmetric leg coordination regardless the breathing conditions and swimming paces, but with high standard deviation (Table 1).

Relationships between impairment, breathing laterality and motor coordination symmetry
Then, multinomial logistic regression was performed based on SI IdC and SI KR predictors, as those predictors contributed significantly to predict the probability of categories to occur when each category was compared to the right physical impairment and right breathing laterality (used as a reference) (Table 2) (X 2 (5) = 39.0, p < 0.001 for SI IdC and X 2 (5) = 38.6,p < 0.001 for SI KR ).Considering AIC, R 2 N and X 2 values, a good model fitting occurred Table 1.Mean and standard deviation (SD) of the stroking parameters and motor coordination for the four breathing conditions and the two swimming paces.3 T: breathing every 3 strokes, A: Apnea, NP: breathing every 2 strokes on the non-preferential side; P: breathing every 2 strokes on the preferential side.www.nature.com/scientificreports/(AIC = 311, R 2 N = 0.274, X 2 (10) = 80.1, p < 0.001).Then, the probability of each category to occur was predicted by the estimated marginal means of SI IdC (Table 3 and Fig. 1) and by the estimated marginal means of SI KR (Table 4 and Fig. 2) showing that the highest probability for the categories included swimmers with "right breathing laterality and right impairment" (Sw 1, 2, 10) and swimmers with "right breathing laterality and left impairment" (Sw 7, 8, 9) was predicted by SI IdC < − 10% (i.e.right arm coordination asymmetry) and by SI KR > 10% (i.e.left leg coordination asymmetry).Moreover, the highest probability for the category included swimmers with "left breathing laterality and left impairment" (Sw 5, 6) was predicted by SI IdC > 10% (i.e.left arm coordination asymmetry) and by SI KR > 10% (i.e.left leg coordination asymmetry).Finally, higher probability for the categories included swimmers with "left breathing laterality and right impairment" (Sw 3, 4), swimmers "left breathing Table 3. Probability of each category to occur predicated by estimated marginal means of SI IdC .SI: symmetry index; IdC: Index of Coordination; SE: standard error; CI: confidence interval; SD: standard deviation.

Discussion
Although able-bodied swimmers switched between symmetric and asymmetric arm coordination 8 and body roll 19 according to the requested breathing conditions (bilateral, frontal snorkel and apnea vs. unilateral), our findings confirmed our first hypothesis suggesting that whatever the breathing conditions, Para swimmers with unilateral physical impairment mainly exhibited motor coordination asymmetry rather than symmetry.In fact, Seifert et al. 8 showed that in national able-bodied swimmers, breathing every two strokes on the preferential breathing side led to asymmetric arm coordination on this preferential breathing side, while breathing every two strokes on the non-preferential breathing side led to asymmetric arm coordination on this non-preferential breathing side, and finally, bilateral breathing and apnea led to symmetric arm coordination.According to Lerda and Cardelli 20 , it was suggested that breathing led to a longer relative duration of the entry and catch phase and a shorter relative duration of the pull phase on the breathing side than on the non-breathing side.Those findings emphasised the influence of breathing conditions on arm coordination asymmetry as national ablebodied swimmers adapted their motor coordination (i.e.arm coordination symmetry vs. asymmetry, and side of asymmetry) according to the breathing conditions.In our current study, arm coordination remained asymmetric regardless breathing conditions, which emphasized the influence of impairment.Based on the study of Lecrivain et al. 21, which demonstrated that forearm amputee swimmer generated 40 to 70% force in comparison to an able-bodied swimmer, it is reasonable to consider that the unaffected side played an important role to propel and to compensate the asymmetry linked to unilateral physical impairment.In 10 × 25 m test incremented in speed, Seifert et al. 12 showed that the physical impairment on one side was associated to arm coordination asymmetry on the same side for 83.6% of the trials.It could be hypothesised that the longer relative duration of the arm propulsive phase on the unaffected side (resulting in arm coordination asymmetry) would ensure the greatest part of the propulsion to compensate the lack of propulsion and balance encountered on the impaired side.This interpretation resonated with the findings of Gonjo et al. 9 in unilateral arm amputee swimmers, showing a larger shoulder roll angle towards the amputee arm side, as shoulder roll asymmetry might be associated to arm coordination asymmetry.Therefore, the longer relative duration of the pull and/or push phases on the impaired side would explain the emergence of arm coordination asymmetry in order to maintain body balance and to ensure propulsion.When physical impairment side and breathing side were considered together, the multinomial logistic regression exhibited a high probability for arm coordination asymmetry to be present in categories of Para swimmers with impairment and breathing laterality on the same side, suggesting the joined effect of unilateral impairment and unilateral breathing (laterality and action).Indeed, Para swimmers of "left impairment & breathing laterality" category (Sw 5, 6) exhibited left arm coordination asymmetry and leg coordination asymmetry, and Para swimmers of "right impairment & breathing laterality" category (Sw 1, 2, 10) exhibited right arm coordination asymmetry and left leg coordination asymmetry.In these two categories in which impairment and breathing laterality were on the same side, we hypothesised that on the breathing side, the arm was responsible for the swimming rhythm and generates higher forces (e.g. the push phase occurs during exhalation on the same side), enabling the swimmer to associate propulsion with unilateral breathing 4,5 and to compensate the unilateral impairment, notably when this impairment was located at the lower-limb level (which was the case for four Para swimmers: Sw 1, 5, 6, 10).As unilateral arm amputation increased the shoulder angle roll on the affected side 9 and as breathing also increased the body roll 17,19,22 , it appeared reasonable to suggest that when unilateral physical impairment and unilateral breathing occurred on the same side, they jointly generated arm coordination asymmetry.
Moreover, unilateral physical impairment and breathing laterality could also occur on different sides and being associated to motor coordination asymmetry.In particular, the multinomial logistic regression showed that "left impairment & right breathing laterality" category (Sw 7, 8, 9) was predicated by high probability of right arm coordination asymmetry and left leg coordination asymmetry.Similarly, the multinomial logistic regression also showed that "right impairment & left breathing laterality" category (Sw 3, 4) was predicated by high probability of left arm coordination asymmetry and right leg coordination asymmetry.Interestingly, the Para swimmers 7 and 9 had left impairment located at lower-limb level, which could explain their left leg coordination asymmetry, and breathed to the right side, which would explain their right arm coordination asymmetry.To sum up, it is interesting to note that both physical impairment and breathing laterality can generate motor coordination asymmetry on different sides and on different limbs (upper vs. lower).This interpretation fits a previous study 23 that observed different ways of coordinating arms and legs in unilateral arm amputee swimmers.
Last, Para swimmers with visual impairment and unilateral breathing preference exhibited either symmetric or asymmetric motor coordination regardless breathing conditions.In particular, the multinomial logistic regression showed that "visual impairment & left breathing laterality" category (Sw 11, 12, 13) was predicated by high probability of left arm coordination asymmetry and by either symmetry or right leg coordination asymmetry, while "visual impairment & right breathing laterality" category (Sw 14, 15) was predicated by high probability of symmetric arm coordination and by either symmetric or right leg coordination asymmetry.Interestingly, the swimmers with visual impairment and left breathing preference (Sw11, Sw12, Sw13) corresponded to a category of our sample with the second highest probability to exhibit left arm coordination asymmetry.Knowing that their breathing preference was to the left side, it could be hypothesized that unilateral breathing contributed to generate arm coordination asymmetry as those Para swimmers had less visual control on arms movement.Indeed, previous studies observed that turning head to breath generated higher body roll on the breathing side 17,19,22 and could disturb the arm stroke organisation 8,22 .However, this interpretation could not be generalized to all swimmers with visual impairment because swimmers Sw14 and Sw15 with visual impairment and right breathing preference remained mainly with arm coordination symmetry.

Arm coordination symmetry
The front crawl arm stroke cycle can be divided into four phases (i.e., catch and glide, pull, push and recovery), for which the relative duration was expressed in % of one arm stroke cycle duration 30 .The catch and glide and recovery are identified as non-propulsive phases while the pull and push are identified as propulsive phases.The full procedure to detect the beginning of pull, push and recovery phases using accelerometric and gyrometric data was extensively previously described 31,32 .The medial-lateral angular velocity of the forearm was filtered with Butterworth low-pass filter with cut-off frequency of 20 Hz and was used to detect the entry of the hand in water 32 .This corresponds to the first observable peak on the raw gyroscopic data between the instant of maximum angular velocity (corresponding to the half arm recovery) and the start of the pull.From there, the duration of one arm stroke cycle (T, in s), corresponding to the absolute time separating one hand water entry to the next entry of the same hand, has been computed and then the arm stroke rate (SR, in Hz) was obtained as follows (Eq.1): Finally, absolute stroke cycle durations were time-normalized (i.e., one complete stroke cycle is 100%) to allow averaging between cycles.
The arm coordination was assessed by the index of coordination (IdC) which quantifies the time gap between the propulsive phases of the two arms 30 .IdC was computed as the mean of IdC left (Eq.2) and IdC right (Eq. 3): (1) SR = 1/T

Table 2 .
Model coefficients for the prediction of each category (Unilateral Physical Impairment I, Visual Impairment VI & Breathing side B) to occur according to SI IdC and SI KR predictors.Confidence Interval (CI), Standard Error (SE), Z-score and p-value.Significant values are in bold.

Table 4 .
Probability of each category to occur predicated by estimated marginal means of SI KR .SI: symmetry index; KR: Kick Rate; SE: standard error; CI: confidence interval; SD: standard deviation.